Sexual behavior in female western lowland gorillas (Gorilla gorilla gorilla): evidence for sexual competition

Previous research in gorillas suggests that females engage in post‐conception mating as a form of sexual competition designed to improve their own reproductive success. This study focused on sexual behaviors in a newly formed group of western lowland gorillas (Gorilla gorilla gorilla) housed at Zoo Atlanta. All females engaged in mating outside their conceptive periods, although there was individual variation in the frequency of the behavior. An analysis of the presence/absence of sexual behavior found females, regardless of reproductive condition, were more likely to engage in sexual behavior on days when other females were sexually active. On these “co‐occurrence” days, females were significantly more likely to solicit the silverback, but copulations did not differ from expectation. The results find further evidence for sexual competition among female gorillas and suggest that this may occur throughout their reproductive cycle rather than only during pregnancy. Am. J. Primatol. 71:587–593, 2009. © 2009 Wiley‐Liss, Inc.     

Food transfers in immature wild western lowland gorillas (Gorilla gorilla gorilla)

The transfer of food items between individuals has been described in primates as serving an informative purpose in addition to supplementing the diet of immature individuals. This behaviour has yet to be described in western lowland gorillas (Gorilla gorilla gorilla), and results are presented here of observations of food transfers in immature gorillas at Mbeli Bai, Republic of Congo. The frequency of food transfers decreased with increasing immature age, while the frequency of independent feeding and processing of food increased. Transfers between mothers and infants were the most frequent, with infants attempting to take items from the mother. These attempts were not always successful and the item was relinquished on less than 50% of attempts. Mothers also took items from their offspring. The results point to the functional significance of food transfers in western lowland gorillas being informational. In a bai environment, where one species forms the majority of a visiting gorilla’s diet despite other species being available, the initiation of food transfers by immatures is proposed to serve the purpose of familiarising them with which species, and which parts of those species, may be eaten.     

Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla)

We explored two hypotheses related to potential differences between sexes in dispersal behaviour in western lowland gorillas (Gorilla gorilla gorilla). Direct observations suggest that immature females have more opportunities to move between breeding groups than immature males. The distribution of kin dyadic relationships within and between groups does not, however, support this hypothesis. At larger geographical scales, dispersal is likely to be easier for males than females because of the solitary phase most blackbacks experience before founding their own breeding group. However, previous work indicates that males settle preferentially close to male kin. By specifically tracing female and male lineages with mitochondrial and Y-chromosomal genetic markers, we found that male gorillas in the 6000 km2 area we surveyed form a single population whereas females are restricted to the individual sites we sampled and do not freely move around this area. These differences are more correctly described as differences in dispersal distances, rather than differences in dispersal rates between sexes (both sexes emigrate from their natal group in this species). Differences in resource competition and dispersal costs between female and male gorillas are compatible with the observed pattern, but more work is needed to understand if these ultimate causes are responsible for sex-biased dispersal distances in western lowland gorillas.     

Postconflict behavior in captive western lowland gorillas (Gorilla gorilla gorilla)

Postconflict (PC) behaviors, including reconciliation and consolation, have been observed in many primate and several nonprimate species. Using the PC-matched control (MC) method, PC behavior was examined in two groups (n=13) of captive western lowland gorillas, a species for which no conflict resolution data have been published. Analyses of 223 conflicts showed significantly more affiliation between former opponents after a conflict when compared to control periods, indicating reconciliation. Results also showed significantly more affiliation between the victim and a third-party after a conflict, indicating consolation. Both solicited and unsolicited consolation were observed. The majority of the affiliative interactions observed for both reconciliation and consolation were social proximity, which suggests that unlike most nonhuman primates, proximity, rather than physical contact, may be the main mechanism for resolving conflicts in western lowland gorillas. PC behavior was not uniform throughout the groups, but rather varied according to dyad type.     

Mitochondrial DNA phylogeography of western lowland gorillas (Gorilla gorilla gorilla)

The geographical distribution of genetic variation within western lowland gorillas (Gorilla gorilla gorilla) was examined to clarify the population genetic structure and recent evolutionary history of this group. DNA was amplified from shed hair collected from sites across the range of the three traditionally recognized gorilla subspecies: western lowland (G. g. gorilla), eastern lowland (G. g. graueri) and mountain (G. g. beringei) gorillas. Nucleotide sequence variation was examined in the first hypervariable domain of the mitochondrial control region and was much higher in western lowland gorillas than in either of the other two subspecies. In addition to recapitulating the major evolutionary split between eastern and western lowland gorillas, phylogenetic analysis indicates a phylogeographical division within western lowland gorillas, one haplogroup comprising gorilla populations from eastern Nigeria through to southeast Cameroon and a second comprising all other western lowland gorillas. Within this second haplogroup, haplotypes appear to be partitioned geographically into three subgroups: (i) Equatorial Guinea, (ii) Central African Republic, and (iii) Gabon and adjacent Congo. There is also evidence of limited haplotype admixture in northeastern Gabon and southeast Cameroon. The phylogeographical patterns are broadly consistent with those predicted by current Pleistocene refuge hypotheses for the region and suggest that historical events have played an important role in shaping the population structure of this subspecies.     

Social structure and life-history patterns in western gorillas (Gorilla gorilla gorilla)

Life-history traits and ecological conditions have an important influence on primate social systems. Most of what we know about the life-history patterns and social structure of gorillas comes from studies of eastern gorillas (Gorilla beringei sp.), which live under dramatically different ecological conditions compared to western gorillas (Gorilla gorilla sp.). In this paper we present new data on western gorilla social structure and life histories from four study sites, and make comparisons with eastern gorilla populations. Data were obtained from two study sites with gorilla groups undergoing the habituation process (Lossi, Democratic Republic of Congo and Bai Hokou, Central African Republic) and two "bai" studies (Maya Nord and Mbeli Bai, Republic of Congo). The size and structure of these groups were similar to those seen in eastern gorillas. However, differences in the occurrence of various group transitions (group formations, changes between one-male and multimale composition, and group disintegrations) exist, and western gorillas notably exhibit much higher rates of male emigration and correspondingly fewer multimale groups compared to mountain gorillas. Certain phenomena have been observed only rarely, including predation by leopards. The preliminary data show no significant differences in birth rates between western gorillas and mountain gorillas. The ecological variability across gorilla habitats likely explains the flexibility in the social system of gorillas, but we need more information on the social relationships and ecology of western gorillas to elucidate the causes for the similarities and differences between western and eastern gorillas on the levels of individuals, social groups, and population dynamics.     

Within-group social relationships among females and adult males in wild western lowland gorillas (Gorilla gorilla gorilla)

Within-group female relationships, and relationships between females and adult males have not been described for wild western lowland gorillas. New data are presented here from Mbeli Bai in the Nouabale-Ndoki National Park, Republic of Congo. Nine groups were observed over a continuous 2-year period, and affiliative and agonistic interactions, as well as time spent by females and adult males in proximity to each other were recorded. Affiliative behavior was extremely rare in the bai, and measures of proximity between individuals were inconclusive because of the small sample sizes. Rates of agonistic interaction among females were highly variable between groups. The majority of agonistic interactions were undecided, and the supplant rate was low. Evidence for an agonistic dominance hierarchy is weak. The data do not support hypotheses that increased frugivory in western lowland gorillas raises levels of within-group contest competition; however, the need for intersite comparisons is stressed. In contrast, rates of agonistic behavior between females and silverback males were higher and more consistent between groups. Agonistic relationships between males and females conformed with patterns seen in mountain gorillas, where male protection from intraspecific aggression is important. The benefit females gain by forming long-term cooperative alliances appears to be small, and is likely outweighed by reproductive advantages associated with male protection.     

The function of loud calls (Hoot Series) in wild western gorillas (Gorilla gorilla)

The use of loud vocal signals to reduce distance among separated social partners is well documented in many species; however, the underlying mechanisms by which the reduction of spacing occurs and how they differ across species remain unclear. Western gorillas (Gorilla gorilla) offer an opportunity to investigate these issues because their vocal repertoire includes a loud, long‐distance call (i.e., hoot series) that is potentially used in within‐group communication, whereas mountain gorillas use an identical call exclusively during intergroup encounters. First, we tested whether the hoot series functions as a contact/separation call. Second, we examined which individuals were more likely to reply and which party was more responsible for decreasing distance to identify the underlying mechanisms and cognitive implications of hoot series. We collected behavioral, spatial, and acoustic data on five adult gorillas over 15 months at the Mondika Research Center (Republic of Congo and CAR). Hoot series are individually distinct calls and given by both male and female gorillas when separated from each other. Following hooting, the distance between separated group members decreased significantly; thus we concluded that western gorillas use this call to reestablish group cohesion. The way in which proximity was achieved depended upon listeners replying or not to the caller. Replies may indicate a conflict between callers about intended travel direction, with vocal interchanges serving to negotiate a consensus. Although the acoustic features of vocal signals are highly constrained in closely related species, our results demonstrate that the function and usage of particular calls can be flexible. Am J Phys Anthropol 155:379–391, 2014. © 2014 Wiley Periodicals, Inc.     

Male genetic structure and paternity in western lowland gorillas (Gorilla gorilla gorilla)

The male dispersal patterns of western lowland gorillas (WLGs, Gorilla gorilla gorilla) are not well understood. To determine whether most silverbacks stay close to their relatives, we analyzed autosomal and Y‐chromosomal microsatellites (STRs) in wild WLGs at Moukalaba, Gabon. We obtained STR genotypes for 38 individuals, including eight silverbacks and 12 adult females in an approximately 40 km² area. Among them, 20 individuals were members of one identified group (Group Gentil; GG), including one silverback and six adult females. The silverback sired all 13 of the offspring in GG and no Y‐STR polymorphism within GG was found, as expected in a one‐male group structure. Over all silverbacks sampled, Y‐STR diversity was high considering the limited sampling area, and silverbacks with similar Y‐STR haplotypes were not always located in nearby areas. Although the misclassification rate of kinship estimates in this study was not negligible, there were no kin dyads among all silverbacks sampled. These results suggest that silverbacks born in the same group do not stay close to each other after maturation. The Y‐STR diversity in this study was similar to that of a previous study conducted in an area that was approximately 150 times larger than our study area. Similarity of WLG Y‐STR diversity between studies at different sampling scales suggests that male gene flow may not be geographically limited. These results suggest that WLG males normally disperse from their natal areas after maturation, at least, in Moukalaba. Am J Phys Anthropol 151:583–588, 2013. © 2013 Wiley Periodicals, Inc.     

Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology

The metabolic activities of gut microbes significantly influence host physiology; thus, characterizing the forces that modulate this micro‐ecosystem is key to understanding mammalian biology and fitness. To investigate the gut microbiome of wild primates and determine how these microbial communities respond to the host's external environment, we characterized faecal bacterial communities and, for the first time, gut metabolomes of four wild lowland gorilla groups in the Dzanga‐Sangha Protected Areas, Central African Republic. Results show that geographical range may be an important modulator of the gut microbiomes and metabolomes of these gorilla groups. Distinctions seemed to relate to feeding behaviour, implying energy harvest through increased fruit consumption or fermentation of highly fibrous foods. These observations were supported by differential abundance of metabolites and bacterial taxa associated with the metabolism of cellulose, phenolics, organic acids, simple sugars, lipids and sterols between gorillas occupying different geographical ranges. Additionally, the gut microbiomes of a gorilla group under increased anthropogenic pressure could always be distinguished from that of all other groups. By characterizing the interplay between environment, behaviour, diet and symbiotic gut microbes, we present an alternative perspective on primate ecology and on the forces that shape the gut microbiomes of wild primates from an evolutionary context.     

Spatial memory and foraging competition in captive western lowland gorillas (Gorilla gorilla gorilla)

Spatial memory and foraging competition were investigated in three mother/offspring pairs of western lowland gorillas,Gorilla gorilla gorilla, using a naturalistic foraging task at the Toronto Zoo. Sixteen permanent food sites were placed throughout the animals’ enclosures. All of the sites were baited and a pair of animals was free to visit the sites and collect the food. Five of the subjects collected the food with accuracy better than chance. Most of the subjects visited the sites using a pattern, and for half the subjects this was one of adjacency. The high accuracy of five of the subjects and the lack of a consistent adjacency pattern suggest that the animals did in fact use spatial memory. Furthermore, the gorillas tended to avoid visiting food sites that had been previously depleted by their partner. They also appeared to split their search of the enclosures, each visiting only a proportion of the food sites. This indicated that the animals were competing and altering their foraging behaviour based on the behaviour of their partner. Therefore, accuracy was recalculated to take this into account. When the sites depleted by either animal in a pair during a given trial were worked into the accuracy calculations for individual animals, three of the animals still maintained accuracy above chance. This suggests that the animals were not only able to remember which sites they had depleted, but those sites depleted by their foraging partner as well.     

Species and sex identification of western lowland gorillas (Gorilla gorilla gorilla), eastern lowland gorillas (Gorilla beringei graueri) and humans

Methods for the identification of the sex and species of individuals from samples non-invasively taken from humans and gorillas were established. Amplification of a segment of amelogenin (AMG), which is an X–Y homologous gene, using two pairs of primers from human AMG, revealed both X- and Y-specific bands. The possibility of sex identification was examined by typing the AMG gene using hair and fecal samples from captive western lowland gorillas (Gorilla gorilla gorilla) in Japan and hair samples from wild eastern lowland gorillas (Gorilla beringei graueri) in the Kahuzi-Biega National Park, Democratic Republic of Congo, which were sexed by direct observation. Species-specific bands of AMG in gorillas and humans were identified by restriction fragment length polymorphisms analysis. These tests could be used for sexing unidentified individuals of wild western and eastern lowland gorillas, and screening contamination of human DNA from non-invasively acquired samples.     

Deception and hiding in captive lowland gorillas (Gorilla gorilla gorilla)

Deception and hiding are described for a group of captive lowland gorillas comprising two adult males, one female, and her infant. The males repeatedly interacted with the infant, and their interest was repeatedly thwarted by the mother. As in other social situations in which one animal controls access to an object desired by another, deceit was used to thwart the other's control. Either one or both males at times concealed their actions toward the infant, inhibited their attention to the infant, created a neutral image to get the infant, or interacted with the infant to tease the mother.     

A training program for noninvasive semen collection in captive western lowland gorillas (Gorilla gorilla gorilla)

Staff at Omaha's Henry Doorly Zoo devised a training program for noninvasive semen collection from three male gorillas. Trained behaviors, shaped using food rewards and verbal praise, enabled the trainer to perform a cursory physical examination and collect >270 semen samples during the study period. Ejaculate volume, sperm motility, and progressive forward motion were recorded. Two of the gorillas regularly produced semen samples that were cryopreserved. Frozen semen from one gorilla was successfully used in an assisted reproductive procedure. The training program may be used as a guideline for other institutions to create similar programs. Zoo Biol 17:143–151, 1998. © 1998 Wiley-Liss, Inc.     

Relative growth,ontogeny, and sexual dimorphism in gorilla(Gorilla gorilla gorilla and G. g. beringei): Evolutionary and ecological considerations

Gorillas are the largest and among the most sexually dimorphic of all extant primates. While gorillas have been incorporated in broad-level comparisons among large-bodied hominoids or in studies of the African apes, comparisons between gorilla subspecies have been rare. During the past decade, however, behavioral, morphological, and molecular data from a number of studies have indicated that the western lowland (Gorilla gorilla gorilla) and eastern mountain (Gorilla gorilla beringei) subspecies differ to a greater extent than has been previously believed. In this study I compare patterns of relative growth of the postcranial skeleton to evaluate whether differences between subspecies result from the differential extension of common patterns of relative growth. In addition, patterns of ontogeny and sexual dimorphism are also examined. Linear skeletal dimensions and skeletal weight were obtained for ontogenetic series of male and female G.g. gorilla (n = 315) and G.g. beringei (n = 38). Bivariate and multivariate methods of analysis were used to test for differences in patterns of relative growth, ontogeny, and sexual dimorphism between sexes of each subspecies and in same-sex comparisons between subspecies. Results indicate males and females of both subspecies are ontogenetically scaled for postcranial proportions and that females undergo an earlier skeletal growth spurt compared to males. However, results also indicate that the onset of the female growth spurt occurs at different dental stages in lowland and mountain gorillas and that mountain gorillas may be characterized by higher rates of growth. Finally, data demonstrate lowland and mountain gorilla females do not differ significantly in adult body size, but mountain gorilla males are significantly larger than lowland gorilla males, suggesting mountain gorillas are characterized by a higher degree of sexual dimorphism in body size. Thus, although lowland and mountain gorillas do not appear to have evolved novel adaptations of the postcranium which correlate with differences in locomotor behavior, the present investigation establishes subspecies differences in ontogeny and sexual dimorphism which may be linked with ecological variation. Specifically, these findings are evaluated in the context of risk aversion models which predict higher growth rates and increased levels of sexual dimorphism in extreme folivores. Am. J. Primatol. 43:1–31, 1997. © 1997 Wiley-Liss, Inc.